Auditory feedback in learning and maintenance of vocal behaviour

Songbirds are one of the best-studied examples of vocal learners. Learning of both human speech and birdsong depends on hearing. Once learned, adult song in many species remains unchanging, suggesting a reduced influence of sensory experience. Recent studies have revealed, however, that adult song is not always stable, extending our understanding of the mechanisms involved in song maintenance, and their similarity to those active during song learning. Here we review some of the processes that contribute to song learning and production, with an emphasis on the role of auditory feedback. We then consider some of the possible neural substrates involved in these processes, particularly basal ganglia circuitry. Although a thorough treatment of human speech is beyond the scope of this article, we point out similarities between speech and song learning, and ways in which studies of these disparate behaviours complement each other in developing an understanding of general principles that contribute to learning and maintenance of vocal behaviour.     

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing,production and learning

Communication between auditory and vocal motor nuclei is essential for vocal learning. In songbirds, the nucleus interfacialis of the nidopallium (NIf) is part of a sensorimotor loop, along with auditory nucleus avalanche (Av) and song system nucleus HVC, that links the auditory and song systems. Most of the auditory information comes through this sensorimotor loop, with the projection from NIf to HVC representing the largest single source of auditory information to the song system. In addition to providing the majority of HVC’s auditory input, NIf is also the primary driver of spontaneous activity and premotor-like bursting during sleep in HVC. Like HVC and RA, two nuclei critical for song learning and production, NIf exhibits behavioral-state dependent auditory responses and strong motor bursts that precede song output. NIf also exhibits extended periods of fast gamma oscillations following vocal production. Based on the converging evidence from studies of physiology and functional connectivity it would be reasonable to expect NIf to play an important role in the learning, maintenance, and production of song. Surprisingly, however, lesions of NIf in adult zebra finches have no effect on song production or maintenance. Only the plastic song produced by juvenile zebra finches during the sensorimotor phase of song learning is affected by NIf lesions. In this review, we carefully examine what is known about NIf at the anatomical, physiological, and behavioral levels. We reexamine conclusions drawn from previous studies in the light of our current understanding of the song system, and establish what can be said with certainty about NIf’s involvement in song learning, maintenance, and production. Finally, we review recent theories of song learning integrating possible roles for NIf within these frameworks and suggest possible parallels between NIf and sensorimotor areas that form part of the neural circuitry for speech processing in humans.     

Repertoire size,auditory templates,and selective vocal learning in songbirds

When vocal variability, here measured by song repertoire size, increases in songbirds, it may become increasingly difficult to encode genetically all the information which is required to ensure the learning of only conspecific songs. Marsh wrens (Cistothorus palustris) have sizeable song repertoires, and while no vocal mimicry is evident in the field, males will readily learn heterospecific songs in the laboratory. These data, together with data from the literature, support the proposed relationship between increased repertoire sizes and reduced specificity of the innate auditory template which guides vocal learning.     

The maintenance of vocal learning by gene-culture interaction: the cultural trap hypothesis

Vocal learning has evolved in several groups of animals, yet the reasons for its origins and maintenance are controversial, with none of the theories put forward appearing to apply over a broad range of species. The theory of gene-culture coevolution is applied to this problem taking the specific case of the maintenance of song learning in birds. The interaction between genes underlying the filter for recognizing and learning conspecific song and the culturally transmitted songs themselves sets up an evolutionary force that may maintain vocal learning. We evaluate this hypothesis using a spatial simulation model. Our results suggest that selection that would maintain song learning exists over a wide range of conditions. Song learning may persist due to an evolutionary trap even though the average fitness in a population of learners may be lower than in a population of non-learners.     

A blueprint for vocal learning: auditory predispositions from brains to genomes

Memorizing and producing complex strings of sound are requirements for spoken human language. We share these behaviours with likely more than 4000 species of songbirds, making birds our primary model for studying the cognitive basis of vocal learning and, more generally, an important model for how memories are encoded in the brain. In songbirds, as in humans, the sounds that a juvenile learns later in life depend on auditory memories formed early in development. Experiments on a wide variety of songbird species suggest that the formation and lability of these auditory memories, in turn, depend on auditory predispositions that stimulate learning when a juvenile hears relevant, species-typical sounds. We review evidence that variation in key features of these auditory predispositions are determined by variation in genes underlying the development of the auditory system. We argue that increased investigation of the neuronal basis of auditory predispositions expressed early in life in combination with modern comparative genomic approaches may provide insights into the evolution of vocal learning.     

The role of vocal individuality in conservation

Identifying the individuals within a population can generate information on life history parameters, generate input data for conservation models, and highlight behavioural traits that may affect management decisions and error or bias within census methods. Individual animals can be discriminated by features of their vocalisations. This vocal individuality can be utilised as an alternative marking technique in situations where the marks are difficult to detect or animals are sensitive to disturbance. Vocal individuality can also be used in cases were the capture and handling of an animal is either logistically or ethically problematic. Many studies have suggested that vocal individuality can be used to count and monitor populations over time; however, few have explicitly tested the method in this role. In this review we discuss methods for extracting individuality information from vocalisations and techniques for using this to count and monitor populations over time. We present case studies in birds where vocal individuality has been applied to conservation and we discuss its role in mammals.     

Song production in auditory mutants of Drosophila: the role of sensory feedback

To test the role of sensory feedback in song production. we analyzed the courtship songs of Drosophila males expressing auditory mutations. We compared the courtship songs of atonal (ato), beethoven (btv) and touch-insensitive-larva-B (tilB) to wild-type songs. These mutations have in common the fact that the chordotonal organs are disrupted. Since chordotonal organs subserve both hearing (in the antenna) and proprioception (from the wing), these two potential routes for sensory feedback are defective in the mutant flies. We measured six song characters: pulse number within a train, inter-pulse interval, pulse duration, sine burst duration, the carrier frequency of the sine song and the relative amplitude of the sine song. Using multivariate analysis, we found significant differences between mutant and normal songs. In addition many mutant flies exhibit an unusual wing position during singing. The results indicate that sensory feedback plays an important role in shaping the courtship song of Drosophila.     

The different roles of social learning in vocal communication

While vocal learning has been studied extensively in birds and mammals, little effort has been made to define what exactly constitutes vocal learning and to classify the forms that it may take. We present such a theoretical framework for the study of social learning in vocal communication. We define different forms of social learning that affect communication and discuss the required methodology to show each one. We distinguish between contextual and production learning in animal communication. Contextual learning affects the behavioural context or serial position of a signal. It can affect both usage and comprehension. Production learning refers to instances where the signals themselves are modified in form as a result of experience with those of other individuals. Vocal learning is defined as production learning in the vocal domain. It can affect one or more of three systems: the respiratory, phonatory and filter systems. Each involves a different level of control over the sound production apparatus. We hypothesize that contextual learning and respiratory production learning preceded the evolution of phonatory and filter production learning. Each form of learning potentially increases the complexity of a communication system. We also found that unexpected genetic or environmental factors can have considerable effects on vocal behaviour in birds and mammals and are often more likely to cause changes or differences in vocalizations than investigators may assume. Finally, we discuss how production learning is used in innovation and invention, and present important future research questions. Copyright 2000 The Association for the Study of Animal Behaviour.     

Comparative study of long-term reduction of high-frequency song syllables in deafened zebra and Bengalese finches: implications for the role of auditory feedback in song maintenance

Auditory feedback is necessary for adult song maintenance in both oscines and psittacines. Although belonging to phylogenically separated orders, deafened adult oscine Bengalese finches and psittacine budgerigars exhibit similarities in certain aspects of song changes. An interesting question is whether these birds share common mechanisms for song maintenance. Therefore, it is important to compare the effects of deafening on adult song patterns among and within orders. Although zebra and Bengalese finches are closely related oscine species, few studies have performed direct, long-term, quantitative comparisons of their songs after deafening because suitable song characteristics have not been identified. Based on our previous findings for Bengalese finch songs, we analyzed zebra finch songs over 9 months after deafening, focusing on changes in the number of syllables categorized according to fundamental frequencies. Deafened zebra finches demonstrated a gradual but significant decrease in high-frequency syllables and a tendency to increase low-frequency syllables, similar to deafened Bengalese finches. Although this change took longer in zebra finches, the altered proportion of syllables eventually stabilized. Results indicated that adult songs show similar aspects after auditory deprivation, and that neural mechanisms involved in the maintenance of high-frequency song syllables, using auditory feedback, may be present in both finches despite species differences.     

The role of transients in auditory processing

Enhancement of auditory transients is well documented in the auditory periphery and mid-brain, and single unit investigations have identified units with responses which may underlie this sensitivity. It is also known that transients are important in psychophysics in, for example, speech comprehension and object recognition and grouping. In this work we use a simple phenomenological model of auditory transient extraction, based on the skewness of the distribution of energy inside a frequency dependent time window, and show that this view is consistent with electrophysiological measurements of auditory brainstem responses. In addition, we present evidence that this representation may provide a positive biological advantage in processing classes of sound that are behaviourlly relevant.     

The role of kinaesthetic feedback in goal-directed movements

The purpose of this study was to investigate the role of kinaesthetic feedback in the control of goal-directed movements. The subjects were qualified basketball and handball players compared to weightlifters as controls. The body measures and the general motor tests verified fit physical condition of the subjects, and detected no sign that would disturb the execution of special motor tests. The special motor tests were free-throw shootings with basketball to the basket, free shootings with handball to a rectangular frame, zigzag dribbling with basketball to 14 m among traffic cones 2 m apart, and stopping at a mark after running to 10 m. These tests were performed both with open eyes and closed eyes. The results of all special motor tests decreased significantly in the lack of visual information. Furthermore, in contrast to the significantly different results obtained from the three different groups with open eyes, these groups produced equally minor results with closed eyes. It is concluded that the practice of goal-directed movement, learned under visual guidance, does not make the kinaesthetic feedback able to compensate the lack of visual input.     

The comparison of motor learning performance with and without feedback

Ten individuals were divided into two feedback and no-feedback groups. The effect of abstract visual feedback was investigated in these two groups. Using eight electroencephalography (EEG) electrodes, the induced event-related desynchronization/synchronization of the EEG of three motor imagery tasks (left hand, right hand, and right foot) was analyzed by wavelet and spatial filtering methods. Linear discriminant analysis was used to classify the three imagery tasks. Each imagery task's total length was set to 3?s and 1?s of it was used for the classification. The classification result was shown to the subjects of the feedback group in a real-time manner as an abstract visual feedback. While the paired t-test of the first and third sessions of the training days confirmed the improvement of the motor imagery learning in the feedback group (p?<?0.01), the motor imagery learning of the no-feedback group was not significant.     

Alpha activity: The influence of unpatterned light input and auditory feedback

The electroencephalographic alpha activity was studied in ten nonpaid healthy volunteers of either sex, 24-to-27 years of age, under the following experimental conditions: in the dark, in the presence of light of various intensity (1-foot candle, 3-foot candle, and 15-foot candle), with and without alpha contingent auditory feedback. Subjects wore light-diffusing goggles that prevented patterned vision throughout the experimental session.The diffuse-light input was found to be devoid of any effect on alpha activity in the absence of auditory feedback. However, during the feedback, the light intensity above 1-foot candle had a significant suppressant effect on alpha activity. This phenomenon can be explained by an interaction between these two modalities. The 40-minute feedback training did not enhance the basic capacity of subjects to produce alpha activity above their own baseline level.     

The role of acetylcholine in learning and memory

Pharmacological data clearly indicate that both muscarinic and nicotinic acetylcholine receptors have a role in the encoding of new memories. Localized lesions and antagonist infusions demonstrate the anatomical locus of these cholinergic effects, and computational modeling links the function of cholinergic modulation to specific cellular effects within these regions. Acetylcholine has been shown to increase the strength of afferent input relative to feedback, to contribute to theta rhythm oscillations, activate intrinsic mechanisms for persistent spiking, and increase the modification of synapses. These effects might enhance different types of encoding in different cortical structures. In particular, the effects in entorhinal and perirhinal cortex and hippocampus might be important for encoding new episodic memories.     

鸣禽发声控制核团内的神经递质及其在发声学习中的作用

神经递质在鸣禽脑中不仅是神经元间信号传递中介物质,还有资料表明它们通过在习鸣敏感期影响发声控制团间的突触联系的形成和突触可塑性,从而对鸣转类型的确定和巩固起重要作用,本文着重介绍了鸣禽发声控制核团内神经递质的分布及变化情况,并就神经递质在发声学习中的作用进行了探讨。     

Temporal population code of concurrent vocal signals in the auditory midbrain

Unique patterns of spike activity across neuron populations have been implicated in the coding of complex sensory stimuli. Delineating the patterns of neural activity in response to varying stimulus parameters and their relationships to the tuning characteristics of individual neurons is essential to ascertaining the nature of population coding within the brain. Here, we address these points in the midbrain coding of concurrent vocal signals of a sound-producing fish, the plainfin midshipman. Midshipman produce multiharmonic vocalizations which frequently overlap to produce beats. We used multivariate statistical analysis from single-unit recordings across multiple animals to assess the presence of a temporal population code. Our results show that distinct patterns of temporal activity emerge among midbrain neurons in response to concurrent signals that vary in their difference frequency. These patterns can serve to code beat difference frequencies. The patterns directly result from the differential temporal coding of difference frequency by individual neurons. Difference frequency encoding, based on temporal patterns of activity, could permit the segregation of concurrent vocal signals on time scales shorter than codes requiring averaging. Given the ubiquity across vertebrates of auditory midbrain tuning to the temporal structure of acoustic signals, a similar temporal population code is likely present in other species.     

The role of WRNIP1 in genome maintenance

WRNIP1 interacts with WRN helicase, which is defective in the premature aging disease Werner syndrome. WRNIP1 belongs to the AAA+ ATPase family and is conserved from Escherichia coli to human. The protein contains an ubiquitin-binding zinc finger (UBZ) domain at the N terminus and an ATPase domain in the middle region. In addition to WRN, WRNIP1 interacts with proteins involved in multiple cellular pathways, including RAD18, monoubiquitylated PCNA, DNA polymerase δ, RAD51, and ATMIN. Mgs1, the yeast homolog of WRNIP1, may act downstream of ubiquitylation of PCNA to mobilize DNA polymerase δ. By contrast, the functions of WRNIP1 in higher eukaryotic cells remain obscure, although data regarding the roles of WRNIP1 in DNA transactions have emerged recently. Here, we first describe the functions of Mgs1 in DNA transaction. We then describe various features of WRNIP1 and discuss its possible roles based on recent studies of the function of WRNIP1.     

The role of maintenance respiration in plant growth

Abstract Plant growth is the balance of photosynthetic gains and respiratory losses, and it is therefore essential to consider respiration in analyses of plant productivity. The partitioning of dark respiratory losses into two functional components, a growth component and a maintenance component, has proved useful. The growth loss is that associated with synthesis of new biomass while the maintenance loss is that associated with maintenance of existing biomass. Experimental evidence indicates that the respiratory cost of maintenance in herbaceous plants is about equal to the cost of growth over a growing season, with daily maintenace expenditures less important in the small, rapidly growing plant but increasing in significance as plant size increases and the relative growth rate decreases. Because it is such a large fraction of the total carbon budget of a plant, any variations in maintenance requirements may result in significant alterations in productivity. In the present work the theoretical and empirical bases of maintenance respiration are described: magnitudes of maintenance expenditures are summarized; and applications to models of plant growth and productivity are discussed. It is concluded that the costs of maintenance should be included in analyses of plant growth.     

The role of feedback in the regulation of erythropoiesis

The review describes the role of positive and negative feedback released through end-products of erythroid cells in the regulation of erythropoiesis.